ABUNDANCE AND COMMUNITY STRUCTURE OF AMMONIA OXIDIZING ARCHAEA AND BACTERIA IN RESPONSE TO PEANUT GROWTH UNDER CONTROLLED CONDITION IN SHANDONG, CHINA

Chao Huang

Biotech Research Center, Shandong Academy of Agricultural Sciences, Ji’nan, 250100, China; Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Ji’nan, 250100, China

Nianfang Xu

Agricultural and Sideline Raw Materials Research Institute on Light Industry of Shandong, Gaomi, 261500, China

Zaiqiu Fu

Agricultural and Sideline Raw Materials Research Institute on Light Industry of Shandong, Gaomi, 261500, China

Botong Sun

Biotech Research Center, Shandong Academy of Agricultural Sciences, Ji’nan, 250100, China; Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Ji’nan, 250100, China

Shengbo You



Deyuan Ma

Biotech Research Center, Shandong Academy of Agricultural Sciences, Ji’nan, 250100, China; Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Ji’nan, 250100, China

Jinhui Yu

Biotech Research Center, Shandong Academy of Agricultural Sciences, Ji’nan, 250100, China; Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Ji’nan, 250100, China


Abstract

Based on a three-year field experiment under controlled condition in Ji’nan, China, the effects of peanut growth on the variation in the abundance and community structure of ammonia oxidizing bacteria (AOB) and Archaea (AOA) before and after peanut growth were investigated through quantitative PCR and cluster analysis of terminal-restriction fragment length polymorphism. Our results show that the community composition of AOA and AOB was greatly affected by the peanut growth leading to the decreased abundance of AOA and increased abundance of AOB. Furthermore, AOA and AOB community structures varied before and after peanut growth. Phylogenetic analysis indicated that all AOA and AOB community sequences were clustered into the uncultured group. Altogether, the results suggested that the abundance of AOA and AOB in soil and their community compositions can be greatly affected by the peanut growth.

Keywords:

archaea, bacteria, peanut, community structure

Ai, C., Liang, G., Sun, J., Wang, X., He, P., Zhou, W. (2013). Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvo-aquic soil. Soil Biol. Biochem., 57, 30–42.

Bal, A.K., Hameed, S., Jayaram, S. (1989). Ultrastructural characteristics of the host-symbiont interface in nitrogen-fixing peanut nodules. Protoplasma, 150, 19–26.

Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., Rauf, P., Huettel, B., Reinhardt, R., Schmelzer, E., Peplies, J., Gloeckner, F.O., Amann, R., Eickhorst, T., Schulze-Lefert, P. (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature, 488, 91–95.

Chen, X., Zhang, L.-M., Shen, J.-P., Wei, W.-X., He, J.-Z. (2011). Abundance and community structure of ammonia-oxidizing archaea and bacteria in an acid paddy soil. Biol. Fertil. Soils, 47, 323–331.

Chen, X.-P., Zhu, Y.-G., Xia, Y., Shen, J.-P., He, J.-Z. (2008). Ammonia-oxidizing archaea: important players in paddy rhizosphere soil? Environ. Microbiol., 10, 1978–1987.

Chen, Y., Xu, Z., Hu, H., Hu, Y., Hao, Z., Jiang, Y., Chen, B. (2013). Responses of ammonia-oxidizing bacteria and archaea to nitrogen fertilization and precipitation increment in a typical temperate steppe in Inner Mongolia. Appl. Soil Ecol., 68, 36–45.

Chen, Y.-L., Hu, H.-W., Han, H.-Y., Du, Y., Wan, S.-Q., Xu, Z.-W., Chen, B.-D. (2014). Abundance and community structure of ammonia-oxidizing archaea and bacteria in response to fertilization and mowing in a temperate steppe in Inner Mongolia. FEMS Microbiol. Ecol., 89, 67–79.

Chu, H., Fujii, T., Morimoto, S., Lin, X., Yagi, K. (2008). Population size and specific nitrification potential of soil ammonia-oxidizing bacteria under long-term fertilizer management. Soil Biol. Biochem., 40, 1960–1963.

Chu, H., Fujii, T., Morimoto, S., Lin, X., Yagi, K., Hu, J., Zhang, J. (2007). Community structure of ammonia-oxidizing bacteria under long-term application of mineral fertilizer and organic manure in a sandy loam soil. Appl. Environ. Microbiol., 73, 485–491.

Dardanelli, M., Angelini, J., Fabra, A. (2003). A calcium-dependent bacterial surface protein is involved in the attachment of rhizobia to peanut roots. Can. J. Microbiol., 49, 399–405.

Di, H.J., Cameron, K.C., Shen, J.P., Winefield, C.S., O’Callaghan, M., Bowatte, S., He, J.Z. (2009). Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat. Geosci., 2, 621–624.

Di, H.J., Cameron, K.C., Shen, J.-P., Winefield, C.S., O’Callaghan, M., Bowatte, S., He, J.-Z. (2010). Ammonia-oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol. Ecol., 72, 386–394.

Feng, H.S, Zhang, S.S, Wan, S.B, Sui, Q.W, Zuo, X.Q. (1993).The variation of nutrient in soil of sequential cropping of peanut and its response to fertilizer. Chinese J. Oil Crop Sci., 2, 55–59.

Francis, C.A., Roberts, K.J., Beman, J.M., Santoro, A.E., Oakley, B.B. (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Nat. Acad. Sci. USA, 102, 14683–14688.

Gleeson, D.B., Müller, C., Banerjee, S., Ma, W., Siciliano, S.D., Murphy, D.V. (2010). Response of ammonia oxidizing archaea and bacteria to changing water filled pore space. Soil Biol. Biochem., 42, 1888–1891.

He, J.-Z., Shen, J.-P., Zhang, L.-M., Zhu, Y.-G., Zheng, Y.-M., Xu, M.-G., Di, H. (2007). Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ. Microbiol., 9, 2364–2374.

Hynes, H.M., Germida, J.J. (2012). Relationship between ammonia oxidizing bacteria and bioavailable nitrogen in harvested forest soils of central Alberta. Soil Biol. Biochem., 46, 18–25.

Kholdebarin, B., Oertli, J.J. (1994). Nitrification: interference by phenolic compounds. J. Plant Nutr., 17, 1827–1837.

Lavin, M., Pennington, R.T., Klitgaard, B.B., Sprent, J.I., de Lima, H.C., Gasson, P.E. (2001). The dalbergioid legumes (Fabaceae): delimitation of a pantropical monophyletic clade. Am. J. Bot., 88, 503–533.

Martens-Habbena, W., Berube, P.M., Urakawa, H., de la Torre, J.R., Stahl, D.A. (2009). Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature, 461, 976–979.

Moore, D.R.E., Waid, J.S. (1971). The influence of washings of living roots on nitrification. Soil Biol. Biochemistry 3, 69–83.

Prakash, O., Pandey, P.K., Kulkarni, G.J., Mahale, K.N., Shouche, Y.S. (2014). Technicalities and glitches of terminal restriction fragment length polymorphism (T-RFLP). Ind. J. Microbiol., 54(3), 255–261.

Protocol of soil test. (2014). Available: http://soiltest.cfans.umn.edu/our-methods/ [date of access: 03.04.2014]

Rotthauwe, J.H., Witzel, K.P., Liesack, W. (1997). The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol., 63, 4704–4712.

Shen, J.-P., Zhang, L.-M., Zhu, Y.-G., Zhang, J.-B., He, J.-Z. (2008). Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ. Microbiol., 10, 1601–1611.

Sher, Y., Zaady, E., Nejidat, A. (2013). Spatial and temporal diversity and abundance of ammonia oxidizers in semi-arid and arid soils: indications for a differential seasonal effect on archaeal and bacterial ammonia oxidizers. FEMS Microbiol. Ecol., 86, 544–556.

Stark, J.M., Firestone, M.K. (1995). Mechanisms for soil moisture effects on activity of nitrifying bacteria. Appl.Environ. Microbiol., 61, 218–221.

Stres, B., Danevčič, T., Pal, L., Fuka, M.M., Resman, L., Leskovec, S., Hacin, J., Stopar, D., Mahne, I., Mandic-Mulec, I. (2008). Influence of temperature and soil water content on bacterial, archaeal and denitrifying microbial communities in drained fen grassland soil microcosms. FEMS Microbiol. Ecol., 66, 110–122.

Sun, X.S., Feng, H.S., Wan, S.B., Zuo, X.Q. (2001). Changes of main microbial strains and enzymes activities in peanut continuous cropping soil and their interactions. Acta Agron. Sin., 1.

Tamura, K., Dudley, J., Nei, M., Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol. Biol. Evol., 24, 1596–1599.

Tourna, M., Freitag, T.E., Nicol, G.W., Prosser, J.I. (2008). Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ. Microbiol., 10, 1357–1364.

Venter, J.C., Remington, K., Heidelberg, J.F., Halpern, A.L., Rusch, D., Eisen, J.A., Wu, D., Paulsen, I., Nelson, K.E., Nelson, W., Fouts, D.E., Levy, S., Knap, A.H., Lomas, M.W., Nealson, K., White, O., Peterson, J., Hoffman, J., Parsons, R., Baden-Tillson, H., Pfannkoch, C., Rogers, Y.-H., Smith, H.O. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304, 66–74.

Verhamme, D.T., Prosser, J.I., Nicol, G.W. (2011). Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J. 5, 1067–1071.

Walker, C.B., de la Torre, J.R., Klotz, M.G., Urakawa, H., Pinel, N., Arp, D.J., Brochier-Armanet, C., Chain, P.S.G., Chan, P.P., Gollabgir, A., Hemp, J., Hügler, M., Karr, E.A., Könneke, M., Shin, M., Lawton, T.J., Lowe, T., Martens-Habbena, W., Sayavedra-Soto, L.A., Lang, D., Sievert, S.M., Rosenzweig, A.C., Manning, G., Stahl, D.A. (2010). Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Nat. Acad. Sci., 107, 8818–8823.

Wu, Y., Lu, L., Wang, B., Lin, X., Zhu, J., Cai, Z., Yan, X., Jia, Z. (2011). Long-term field fertilization significantly alters community structure of ammonia-oxidizing bacteria rather than archaea in a paddy soil. Soil. Sci. Soc. Am. J. 75, 1431–1439.

Yao, H., Gao, Y., Nicol, G.W., Campbell, C.D., Prosser, J.I., Zhang, L., Han, W., Singh, B.K. (2011). Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl. Environ. Microbiol., 77, 4618–4625.

Zhang, L.-M., Hu, H.-W., Shen, J.-P., He, J.-Z. (2012). Ammonia-oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acidic soils. ISME J., 6, 1032–1045.

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Published
2019-12-17



Chao Huang 
Biotech Research Center, Shandong Academy of Agricultural Sciences, Ji’nan, 250100, China; Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Ji’nan, 250100, China
Nianfang Xu 
Agricultural and Sideline Raw Materials Research Institute on Light Industry of Shandong, Gaomi, 261500, China
Zaiqiu Fu 
Agricultural and Sideline Raw Materials Research Institute on Light Industry of Shandong, Gaomi, 261500, China
Botong Sun 
Biotech Research Center, Shandong Academy of Agricultural Sciences, Ji’nan, 250100, China; Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Ji’nan, 250100, China
Shengbo You 
Deyuan Ma 
Biotech Research Center, Shandong Academy of Agricultural Sciences, Ji’nan, 250100, China; Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Ji’nan, 250100, China
Jinhui Yu 
Biotech Research Center, Shandong Academy of Agricultural Sciences, Ji’nan, 250100, China; Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Ji’nan, 250100, China



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